RESEARCH ARTICLE Open Access

Risk factors of rotavirus diarrhea in hospitalizedchildren in Sanglah Hospital, Denpasar: aprospective cohort studyHendra Salim1*, I Putu Gede Karyana1†, I Gusti Ngurah Sanjaya-Putra1†, Soetjiningsih Budiarsa2† and Yati Soenarto3†

Abstract

Background: Diarrhea is a major public health concern throughout the world because the prevalence of morbidityof diarrhea has not changed significantly in the past decade. It remains the third leading cause of death amongchildren less than 5 years of age. Recent surveillance studies have shown that rotavirus is a significant cause ofpediatric hospitalization and death due to diarrhea. Indonesia has limited data on risk factors, disease burden, anddeaths in children due to rotavirus diarrhea. The objective of this study was to examine the above mentionedfactors related to rotavirus diarrhea in hospitalized children in Sanglah Hospital, Denpasar.

Methods: A prospective cohort study was conducted at Sanglah Hospital Denpasar from April 2009 to December2011. The present study was part of a nationwide study on Extension for Hospital-based Surveillance and StrainCharacterization of Rotavirus Diarrhea Indonesia involving four hospitals throughout Indonesia as a part of the AsianRotavirus Surveillance Network. We studied children aged <5 years who were hospitalized with acute diarrhea, andanalyzed their stool samples using an immunoassay that detects the rotavirus antigen.

Results: A total of 656 patients met the inclusion criteria for this study. Of 5805 patients under the age of 5 whowere hospitalized between April 2009 and December 2011, the prevalence of diarrhea among hospitalized pediatricpatients was 11.3% and the prevalence of rotavirus diarrhea was 49.8%. The male to female ratio of those affectedby rotavirus was 1.6:1. The occurrence of vomiting was significantly higher in rotavirus diarrhea than in non-rotavirusdiarrhea (RR, 1.4; 95% CI, 1.08 to 1.70; p = 0.004).

Conclusions: Diarrhea remains an important cause of hospitalization in children, and rotavirus was the mostimportant etiology. We found that boys had a greatest risk of rotavirus infection than girls. Good nutritional statusand breastfeeding provided the same protection against rotavirus and non-rotavirus diarrhea.

Keywords: Acute diarrhea, Rotavirus, Children

BackgroundRotavirus is recognized as a major cause of non-bacterialgastroenteritis (infection of the stomach and intestinaltract leading to diarrhea and vomiting) especially ininfants and young children worldwide [1,2]. Rotavirusgastroenteritis is endemic worldwide. The infection isassociated with high rate of morbidity throughout theworld and a high rate of mortality in developing coun-tries. It account for more than 800,000 child deaths per

year due to poor nutrition and health care in developingcountries [3].Diarrhea has been estimated to cause 1.5 million

deaths and 21% of deaths worldwide in children underthe age of 5 [4]. In India, most cases of diarrhea (98%)occurred during the first 2 years of life, peaking at 9–11months [2]. Based on a literature review of studies pub-lished between 1986 and 1999 on childhood deathscaused by diarrhea and hospitalizations due to rotavirus,it was estimated that 440,000 annual deaths in childrenaged <5 years occur because of rotavirus infection [1].An estimated 527,000 children aged <5 years died fromrotavirus infection in 2004 with > 85% of these deaths in

* Correspondence: misionarispelayanan@yahoo.com†Equal contributors1Division of Gastroenterology and Hepatology, Department of Child Health,Medical School, Udayana University/Sanglah Hospital, Denpasar, IndonesiaFull list of author information is available at the end of the article

© 2014 Salim et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the CreativeCommons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, andreproduction in any medium, provided the original work is properly credited. The Creative Commons Public DomainDedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article,unless otherwise stated.

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South-East Asia and sub-Saharan Africa [5]. Of 8929Indonesian children in Purworejo district and Yogyakartacity hospitalized between August 2001 and April 2004,16% presented with acute gastroenteritis, and 53% of the1321 tested stool samples were positive for rotavirus [6].This study involved children aged <5 years who were

admitted with diarrhea in Sanglah Hospital, and the aimswere to determine the prevalence of acute diarrhea andthe rotavirus disease, and to determine the risk factorsfor rotavirus diarrhea.

MethodsWe conducted a prospective cohort study from April 2009to December 2011 of hospitalized children with acute diar-rhea. The study was a part of the study on Extension forHospital-based Surveillance and Strain Characterization ofRotavirus Diarrhea Indonesia involving four hospitalsthroughout Indonesia as part of the Asian RotavirusSurveillance Network.For the sample size, we used a risk ratio of 1.1, α = 0.05,

β = 0.2, and the proportion of individuals exposed to theoutcome was 91%. The minimal sample size required was494 patients. This study was approved by the Medicaland Health Research Ethics Committee of the Faculty ofMedicine, Gadjah Mada University, and parents’ writtenconsent was obtained for participation in this study.The study group included patients less than 5 years of

age hospitalized with acute diarrhea. Patients admittedwith diarrhea lasting more than 7 days and those withchronic diarrhea due to malabsorption and structural mal-formations were excluded from the study. We excludeddiarrhea lasting more than 7 days because prolonged orpersistent diarrhea are not usually caused by rotavirus.The parents were questioned about the chief complaints

and the degree of dehydration was examined. Parents weregiven a sterile screw-capped plastic container for collec-tion of stool specimen within 24 hours after admission.A standardized clinical form was completed to obtaindetailed information on the date of admission, age andsex of the patient, nutritional status, previous treatment,hydration status, symptoms, and final diagnosis.For this study, we defined acute diarrhea as >3 loose

stools within a 24-hour period [7] with a duration <7days, and prolonged diarrhea was defined as an illnesslasting between 7 and 14 days [8-10]. Vomiting was de-fined as the forceful expulsion of gastric contents at leastonce in a 24-hour period. Fever was defined by the pres-ence of an axillary temperature greater than or equal to38°C. If present, dehydration was graded as mild (drymucus membranes, decreased tears and urine output),moderate (decreased skin turgor), or severe (excessivelydecreased skin turgor, tachycardia, low blood pressure,anuria, absence of tears) [11]. Breastfeeding was definedas provision of breast milk, either directly from the

breast or expressed, and may constitute any portion ofthe infant’s diet.A sufficient amount of whole stool specimen (5–10 ml)

was collected for all admitted cases in a sterile screw-capped plastic container. Stool samples were divided intwo sets: one was used for routine stool examination andthe other was transported in refrigerated boxes to theMicrobiology Laboratory at Gadjah Mada University,Faculty of Medicine, in Yogyakarta. It was stored at 4–8°C until laboratory testing for rotavirus. In the labora-tory, the sample was aliquoted and stored at −70°C.Rotavirus was detected using an enzyme immuno-assay for rotavirus (Dakopatts®, Dako Diagnostics Ltd.,United Kingdom) in accordance with the manufacturer’sinstructions.Data were entered by a single investigator into the

database that consists of information about clinicalvariables and rotavirus test results. Statistical analysiswas performed using the SPSS 16.0 program. The finaldata were analyzed using the chi-square test and riskratio to determine the significance of relevant parame-ters. The chi-square test was used with 95% confidenceinterval.

ResultsPatient demographics, clinical characteristics and labora-tory findings are listed in Tables 1 and 2. Of the 656 cases,577 (88.0%) had mild to moderate dehydration and 24(3.7%) had severe dehydration. Two patients died and thecase fatality rate was 0.3%. Of the 5805 patients below theage of 5 years who were admitted between April 2009 andDecember 2011, the prevalence of diarrhea was 11.3% andthe prevalence of rotavirus infection in these hospitalizedpatients was 49.8%.This study found an association between the occur-

rence of rotavirus and chief complain on admission, de-gree of dehydration, presence of vomiting (Table 2), and

Table 1 Patient characteristics

Characteristics Total (n = 656)

Sex, male, n (%) 400 (61.0)

Age, median (IQR) month 12.8 (7.5-20.4)

Weight, median (IQR) kg 8.5 (7-10)

Height, median (IQR) cm 75 (66-84)

Degree of dehydration, n (%)

No dehydration 55 (8.4)

Mild-moderate 577 (88.0)

Severe 24 (3.7)

Length of stay, median (IQR) day 3 (3-4)

Rotavirus positive, n (%) 327 (49.8)

IQR = Interquartile range.

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sex (Table 3), but no association was seen between rota-virus infection and nutritional status, breastfeeding, symp-toms of seizure, fever, and hand washing behavior.A multivariate analysis showed that nutritional sta-

tus, capability to eat by him/herself, fed by parent,

breastfeeding, and bottle-feeding were protective factorsfor rotavirus diarrhea, but these results were not statisti-cally significant (Table 4). This study showed that rotavirusdiarrhea was more frequent in boys than girls (adjustedRR, 1.4; 95% CI, 1.04 to 1.97; p = 0.03).

Table 2 Clinical manifestations in children with rotavirus and non-rotavirus diarrhea

Variables Rotavirus positive (n = 327) Rotavirus negative (n = 329) RR (95% CI), p value

Chief complain, n (%)

- Diarrhea 302 (92.4) 276 (83.9) 1.0 (Referent group)

- Vomiting 9 (2.8) 21 (6.4) 1.7 (1.00 to 3.02), 0.017

- Others 16 (4.9) 32 (9.7) 1.6 (1.04 to 2.36), 0.012

General condition at admission, n (%)

- Well 155 (47.4) 150 (45.6) 1.0 (Referent group)

- Irritable 155 (47.4) 155 (47.1) 1.0 (0.87 to 1.19), 0.84

- Lethargy 17 (5.2) 24 (7.3) 1.2 (0.84 to 1.79), 0.26

Degree of dehydration, n (%)

- No dehydration 17 (5.2) 38 (11.6) 1.0 (Referent group)

- Mild-moderate 299 (91.4) 278 (84.5) 0.6 (0.40 to 0.89), 0.03

- Severe 11 (3.4) 13 (4.0) 0.7 (0.38 to 1.21), 0.20

Vomiting, n (%) 275 (84.1) 247 (75.1) 1.4 (1.08 to 1.70), 0.004

Seizure, n (%) 23 (7.0) 30 (9.1) 0.9 (0.63 to 1.18), 0.33

Fever, n (%) 203 (62.1) 195 (59.3) 1.1 (0.90 to 1.24), 0.46

Bloody diarrhea, n (%) 1 (0.3) 7 (2.1) 4.0 (0.64 to 25.22), 0.07*

Outcome, n (%)

- Recovered 319 (97.6) 319 (97.0) 1.0 (Referent group)

- Referral/Death 8 (2.4) 10 (3.0) 1.1 (0.67 to 1.90), 0.64

*Fisher’s exact test.

Table 3 Risk factors for children with rotavirus and non-rotavirus diarrhea

Variables Rotavirus positive (n = 327) Rotavirus negative (n = 329) RR (95% CI), p value

Sex, Male, n (%) 214 (65.4) 186 (56.5) 1.2 (1.03 to 1.43), 0.019

Age, n (%) month

0 – <3 19 (5.8) 22 (6.2) 1.0 (Referent group)

3 – <6 34 (10.4) 35 (10.6) 0.9 (0.63 to 1.41), 0.77

6 – <12 93 (28.4) 89 (27.1) 0.9 (0.63 to 1.30), 0.58

12 – <24 129 (39.4) 109 (33.1) 0.9 (0.60 to 1.21), 0.35

24 – <36 33 (10.1) 45 (13.7) 1.1 (0.72 to 1.67), 0.67

36 – <48 12 (3.7) 15 (4.6) 1.0 (0.61 to 1.78), 0.88

48 – <60 7 (2.1) 14 (4.3) 1.4 (0.70 to 2.77), 0.33

Nutritional status, n (%)

Well-nourish 231 (70.6) 221 (67.2) 1.0 (Referent group)

Malnourish 96 (29.4) 108 (32.8) 1.1 (0.92 to 1.29), 0.34

Family member with diarrhea, n (%) 37 (11.3) 26 (7.9) 1.2 (0.96 to 1.50), 0.14

Eat by him/herself, n (%) 73 (22.3) 83 (25.2) 0.9 (0.76 to 1.11), 0.38

Fed by parent, n (%) 101 (30.9) 111 (33.7) 0.9 (0.79 to 1.11), 0.43

Breastfeeding, n (%) 125 (38.3) 122 (37.1) 1.0 (0.88 to 1.20), 0.76

Bottle-feeding, n (%) 245 (74.9) 245 (74.5) 1.0 (0.85 to 1.21), 0.89

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DiscussionDiarrheal disease remains a significant health problem inmany parts of the world [12]. Rotavirus is an importantcause of diarrhea and contributes significantly to diar-rhea in both developing and developed countries [13]. InNepal, rotavirus accounts for up to 38% of diarrhea inchildren less than 5 years old [12]. In the 43 countriesparticipating in the global surveillance network for rota-virus in 2009, 36% of hospitalizations for diarrhea amongchildren aged <5 years were caused by rotavirus infec-tion. Surveillance of the period between 2001 and 2008revealed a detection rate of 40% in 35 countries with thevirus distributed in similar regions [14]. The presentstudy revealed that rotaviruses are important etiologicagents of acute diarrhea, accounting for 49.8% of allcases of acute gastroenteritis.Rotavirus was detected in a higher proportion of males

than females (RR, 1.2; 95% CI, 1.03 to 1.43; p = 0.019),indicating that males had a higher rotavirus stool excre-tion rate than females [3]. The male to female ratio ofrotavirus infection was 1.6:1. This is in agreement withthe finding that boys are twice more susceptible to rota-virus infection than girls and are more likely to be hospi-talized [15]. Junaid et al. reported that the ratio was 1.8:1in Nigeria, while Samir et al. and Puri et al. reported ra-tios of 1.5:1 and 1:2.4 for Bahrain and India, respectively[3]. According to the WHO scientific group [13,16], thenumber of affected males was up to 20% higher than thenumber of females in some studies, but it is not known

whether this is due to a greater susceptibility to rotavirusexposure in boys or a greater likelihood of parents of af-fected boys seeking medical care.According to the WHO scientific working group [13,16],

most cases of rotavirus infections occur in children be-tween 6 and 24 months with a peak incidence at 9 to 12months. A surveillance conducted in 6 hospitals in 6provinces of Indonesia found that children aged <3months are less likely to have rotavirus diarrhea. Ourfindings confirmed that children aged <3 months are lesssusceptible to rotavirus, and children between 6 and 24month are highly susceptible to rotavirus diarrhea.Rotavirus is spread by direct person-to-person contact.

Effective hand washing and disposal or disinfection ofcontaminated items are important measures in the pre-vention of rotavirus infection. Breastfeeding reducesgastrointestinal infections as breast milk contains lactad-herin that is protective against symptomatic rotavirus in-fection. Lactadherin, secretory IgA, T-and B-lymphocytes,bactericidal lactoferrin, oligosaccharides and human milkglycans in breast milk protect the intestinal epitheliumagainst pathogens. Human milk also contains anti-rotavirus antibodies that seem to play a smaller roleagainst pathogens. Current WHO guidelines on themanagement of diarrhea recommend continued breast-feeding during a diarrhea episode [4].One study asserted that transplacentally acquired

immunoglobulin G antibodies and immunoglobulin Ain breastmilk protect children aged <3 months againstrotavirus infection. Human breast milk contains othercomponents, including milk mucin, which have beenshown to inhibit rotavirus replication and infection bybinding to the virus [17,18].A prospective study by Naficy et al. found a lower inci-

dence of rotavirus diarrhea in infants that received breastmilk [19]. Duffy et al. [20] followed a cohort of 197 infantsand found no difference in rotavirus infection rates be-tween the breast-fed and bottle-fed infants. Furthermore,a study by Wobudeya et al. [4] failed to show that breast-feeding was protective against rotavirus diarrhea in infants.Our study found no difference in rotavirus infection ratesbetween bottle-fed and non-bottle-fed infants.

Table 4 Multivariate analysis of risk factors for rotavirusdiarrhea

Variables Regressioncoefficient

Adjusted RR (95% CI),p value

Sex 0.361 1.4 (1.04 to 1.97), 0.03

Nutritional status −0.117 0.9 (0.64 to 1.24), 0.50

Family member with diarrhea 0.404 1.5 (0.88 to 2.55), 0.14

Eat by him/herself −0.100 0.9 (0.60 to 1.36), 0.63

Fed by parent −0.094 0.9 (0.65 to 1.28), 0.59

Breastfeeding −0.052 0.9 (0.68 to 1.33), 0.76

Bottle-feeding −0.028 0.9 (0.66 to 1.44), 0.89

Figure 1 Comparison of symptoms of fever and vomiting between rotavirus and non-rotavirus diarrhea.

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The close relationship between age, breastfeeding androtavirus diarrhea could probably explain the observationsin these reports. The peak age for rotavirus diarrhea is6–11 months while the rates of breastfeeding begin todecline after 6 months. The protective effects of breast-feeding seem to wane with age [4]. This might explainwhy studies that focused on infants 6 months or youngertended to show the protective effect of breastfeeding.Vomiting appears to be more common in children

with rotavirus diarrhea than those with non-rotavirusdiarrhea [3]. The present study found that 83.3% of hos-pitalized children with rotavirus diarrhea presented withvomiting (RR, 1.4; 95% CI, 1.08 to 1.70, p = 0.004). Theoccurrence of the symptoms of diarrhea, fever and vomit-ing was significantly different between children with rota-virus diarrhea and those with non-rotavirus diarrhea [3].The present study found that 54.1% of cases of rotavirusdiarrhea presented with both fever and vomiting (Figure 1).These symptoms could increase the risk of dehydrationand hospitalization. Although there appears to be an in-creasing trend in admitting young children with diarrhea,this appears to be associated with a low mortality, possiblybecause of better hospital clinical management [6].Rotavirus diarrhea occurs year round but there is an

apparent increase in the prevalence of rotavirus infectionin the cool, dry season. A study in Indonesia showed aclear seasonal trend of rotavirus infection in the hot anddry seasons with low humidity [6,17]. Another study inIndia found that 64.8% of rotavirus cases occurred inthe cooler months i.e., from November to January. Thepresent study found no consistent pattern in the num-ber of rotavirus cases in 2 consecutive years (Figure 2).We assume that rotavirus diarrhea requiring hospitaladmission occur year round without any seasonal trend.This study has several limitations, such as the stool

specimen of the diarrhea cases were not cultured, so wedid not know the characterization of the non-rotavirusdiarrhea that may be consisting of both viral non-rotavirus and non-viral diarrhea. This study also did not

include outpatient children; therefore we did not knowthe burden and risk factors for all rotavirus diarrhea inDenpasar.

ConclusionsThe prevalence of diarrhea at Sanglah Hospital was 11.3%.The prevalence of rotavirus diarrhea was 49.8%. The re-sults of this study confirmed that diarrhea remains animportant cause of hospitalization in children, and rota-virus was the most important etiology of diarrhea. Thepeak prevalence was between 6 and 24 months of age.We also found that boys were more susceptible to rota-virus infection than girls. Rotavirus diarrhea in hospital-ized children was manifested as fever and vomitingmore often than one symptom alone. In these children,good nutritional status and breastfeeding provided thesame protection against rotavirus and non-rotavirusdiarrhea.

AbbreviationsIQR: Interquartile range; WHO: World Health Organization.

Competing interestsThe authors declare that they have no competing interests.

Authors’ contributionsAll authors read and approved the final manuscript. HS participated in thedesign of the study, data collection, statistical analysis, and helped draft themanuscript. SB and YS participated in the design of the study, datacollection, and helped draft the manuscript. IPGK participated in datacollection and helped draft the manuscript. IGNSP participated in the designof the study and helped draft the manuscript.

Authors’ informationHS is the Master of Biomedicine and pediatric researcher in the Departmentof Child Health, Medical School, Udayana University/Sanglah Hospital.IPGK and IGNSP are pediatric gastroenterology consultants and researchersin the Department of Child Health, Medical School, Udayana University/Sanglah Hospital.SB is the Professor of Child Growth and Development – Social Pediatrics inthe Department of Child Health, Medical School, Udayana University/SanglahHospital.YS is the Professor of Pediatric Gastroenterology in the Department of ChildHealth, Medical School, Gadjah Mada University/Sardjito Hospital. She is theproject head of Extension for Hospital-based Surveillance and StrainCharacterization of Rotavirus Diarrhea Indonesia.

Figure 2 Seasonal variation in rotavirus positivity.

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AcknowledgementsWe thank Sukanto, IP. (PT Bio Farma) for the laboratory work; and AbdulWahab and Althaf Setyawan (Community Health and Nutrition ResearchLaboratory, Faculty of Medicine, Gadjah Mada University) for data analysis.We also thank doctors, nurses, administrative staff and research assistants inthe Department of Child Health, Faculty of Medicine, Udayana University/Sanglah Hospital for their help in this study.

Funding sourceSalary and/or intellectual support was provided by WHO Regional Office forSouth East Asia (SEARO) to all authors during this study.

Financial disclosureThe authors have no financial relationships to disclose that are relevant tothis article.

Author details1Division of Gastroenterology and Hepatology, Department of Child Health,Medical School, Udayana University/Sanglah Hospital, Denpasar, Indonesia.2Division of Child Growth and Development – Social Pediatrics, Departmentof Child Health, Medical School, Udayana University/Sanglah Hospital,Denpasar, Indonesia. 3Division of Gastroenterology and Hepatology,Department of Child Health, Medical School, Gadjah Mada University/SardjitoHospital, Yogyakarta, Indonesia.

Received: 24 December 2013 Accepted: 19 March 2014Published: 26 March 2014

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doi:10.1186/1471-230X-14-54Cite this article as: Salim et al.: Risk factors of rotavirus diarrhea inhospitalized children in Sanglah Hospital, Denpasar: a prospectivecohort study. BMC Gastroenterology 2014 14:54.

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